The Spatial Organization of Ascending Auditory Pathway Microstructural Maturation From Infancy Through Adolescence Using a Novel Fiber Tracking Approach

Abstract

Auditory perception is established through experience-dependent stimuli exposure during sensitive developmental periods; however, little is known regarding the structural development of the central auditory pathway in humans. The present study characterized the regional developmental trajectories of the ascending auditory pathway from the brainstem to the auditory cortex from infancy through adolescence using a novel diffusion MRI-based tractography approach and along-tract analyses. We used diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) to quantify the magnitude and timing of auditory pathway microstructural maturation. We found spatially varying patterns of white matter maturation along the length of the tract, with inferior brainstem regions developing earlier than thalamocortical projections and left hemisphere tracts developing earlier than the right. These results help to characterize the processes that give rise to functional auditory processing and may provide a baseline for detecting abnormal development.

Keywords: NODDI; auditory pathway; child development; microstructure; tractography; white matter.

FIGURE 1

Age distribution of subjects included in the study stratified by sex. F = female and M = male.

FIGURE 2

Auditory pathway anatomy. (A) Schematic of the ascending auditory pathway. (B) Tractography of the lower (blue) and upper (red) auditory pathways is shown on a coronal slice of a subject FA map overlaid with intravoxel multitensor models. (C) An axial slice shows the upper auditory pathway projects through the medial geniculate nucleus of the thalamus. (D) A sagittal slice shows the auditory pathway from the cochlear nerve to the inferior colliculus (white sphere). (E) An axial slice shows the complex fiber orientations at the level of the pons.

FIGURE 3

Age‐related changes in auditory pathway microstructure are shown for the left and right upper and lower auditory pathways for DTI parameters (FA, AD, RD, and MD) and NODDI (NDI and ODI). The fitted line for each parameter and tract reflects the best fit model, where blue denotes linear regression and black denotes exponential changes. For models that demonstrate exponential age‐related changes, the age at 90% of the asymptotic value is shown with a dashed red line.

FIGURE 4

Regional variation in the developmental timing of diffusion microstructure within the auditory pathway. The age at 90% of the asymptotic value of the fitted Brody growth curve for each point along the auditory pathway is shown for (A) AD, (B) MD, (C) NDI, (D) RD, and (E) FA. Regions shaded in gray denote points where a growth curve did not provide the best fit model using BIC. L—left and R—right.

FIGURE 5

Regional linear maturation of microstructural parameters within the auditory pathway. The estimated slope (β) is provided at points along the auditory pathway for (A) FA and (B) NDI where the linear model provided the best fit model. Regions shaded in gray denote points where the linear model did not provide the best fit using BIC. Note that FA in the bilateral vestibulocochlear nerve was not significantly associated with age using either a linear model or Brody growth curve. L—left and R—right.

FIGURE 6

Exponential growth curve error estimates for regional auditory pathway microstructural maturation. The standard error (SE) of the exponential growth rate (k) is provided for parameters along the auditory pathway obtained through bootstrapping with replacement. Regions shaded in gray denote points where the growth curve did not provide the best fit model. The SE is provided for the same regions shown in Figure 4. L—left and R—right.

FIGURE 7

Standard error (SE) for the slope (β) estimated with a linear model for diffusion parameters at points along the auditory pathway. Regions in gray denote points where the linear model did not provide the best fit model. The SE is provided for the same regions shown in Figure 5. L—left and R—right.

FIGURE 8

Regional lateralization of microstructural maturation within the auditory pathway. The developmental laterality index (dLI) for the age at 90% of α estimated using a Brody growth curve is provided for (A) AD, (B) MD, and (C) RD. Red (positive dLI) denotes regions that develop later on the right side, while blue (negative dLI) denotes regions that mature earlier on the right side. Regions denoted as gray do not have a strongly preferred lateralization. L—left and R—right.